H2O2 in plant peroxisomes: An in vivo analysis uncovers a Ca2+-dependent scavenging system

Plant Journal

Volumn 62, Issue 5, 2010, Pages 760-772

  Costa, Alex ^a   Drago, Ilaria ^a   Behera, Smrutisanjita ^a   Zottini, Michela ^a   Pizzo, Paola ^a   Schroeder, Julian I ^b   Pozzan, Tullio ^a,c   Schiavo, Fiorella Lo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

Author keywords

Calcium; Cameleon; Hydrogen peroxide; HyPer; Plant peroxisomes

Indexed keywords

ARABIDOPSIS PLANT; CAMELEON; CATALASE ACTIVITY; FLUORESCENCE RATIO; GAIN INSIGHT; GREEN FLUORESCENT PROTEIN; HYPER; IN-PLANTS; IN-VIVO; IN-VIVO ANALYSIS; NON-INVASIVE; PLANT PEROXISOMES; REACTIVE OXYGEN SPECIES; SCAVENGING EFFICIENCY; SIGNALLING PATHWAYS; SPECIFIC COMPONENT; SUBCELLULAR COMPARTMENTS;

CALCIUM; FLUORESCENCE; HYDROGEN PEROXIDE; OXIDATION; OXYGEN; PLANT CELL CULTURE; PLANTS (BOTANY);

CYTOLOGY;

ARABIDOPSIS; NICOTIANA TABACUM;

CALCIUM; GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; PLANT RNA;

ARABIDOPSIS; ARTICLE; CULTURE TECHNIQUE; METABOLISM; OXIDATIVE STRESS; PEROXISOME; PLANT LEAF; TRANSGENIC PLANT;

ARABIDOPSIS; CALCIUM; CELL CULTURE TECHNIQUES; GREEN FLUORESCENT PROTEINS; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PEROXISOMES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; RNA, PLANT;

EID: 77952835052     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04190.x     Document Type: Article

References (50)

1. Allen, G.J., Kwak, J.M., Chu, S.P., Llopis, J., Tsien, R.Y., Harper, J.F. Schroeder, J.I. (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J. 19, 735 747.
2. Allen, G.J., Chu, S.P., Harrington, C.L., Schumacher, K., Hoffmann, T., Tang, Y.Y., Grill, E. Schroeder, J.I. (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature, 411, 1053 1057.
3. Apel, K. Hirt, H. (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant. Biol. 55, 373 399.
4. Asada, K. Takahashi, M. (1987) Production and scavenging of active oxygen in photosynthesis. In Photoinhibition (Kyle, D.J., Osborne, C.B. Arntzen, C.J., eds).
5. Baker, A. Graham, I.A. (2002) Plant Peroxisomes. Biochemistry, Cell Biology and Biotechnological Applications.
6. Batoko, H., Zheng, H.Q., Hawes, C. Moore, I. (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell, 12, 2201 2218.
7. Belousov, V.V., Fradkov, A.F., Lukyanov, K.A., Staroverov, D.B., Shakhbazov, K.S., Terskikh, A.V. Lukyanov, S. (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods, 3, 281 286.
8. Bienert, G.P., Schjoerring, J.K. Jahn, T.P. (2006) Membrane transport of hydrogen peroxide. Biochim. Biophys. Acta, 1758, 994 1003.
9. Bienert, G.P., Møller, A.L., Kristiansen, K.A., Schulz, A., Møller, I.M., Schjoerring, J.K. Jahn, T.P. (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183 1192.
10. Corpas, F.J., Palma, J.M., Sandalio, L.M., López-Huertas, E., Romero-Puertas, M.C., Barroso, J.B. del Río, L.A. (1999) Purification of catalase from pea leaf peroxisomes: identification of five different isoforms. Free Radic. Res. 31, S235 S241.
11. Corpas, F.J., Barroso, J.B. del Río, L.A. (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci. 6, 145 150.
12. + channels necessary for development? Plant Mol. Biol. 54, 837 852.
13. Dammann, C., Ichida, A., Hong, B., Romanowsky, S.M., Hrabak, E.M., Harmon, A.C., Pickard, B.G. Harper, J.F. (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol. 132, 1840 1848.
14. Drago, I., Giacomello, M., Pizzo, P. Pozzan, T. (2008) Calcium dynamics in the peroxisomal lumen of living cells. J. Biol. Chem. 283, 14384 14390.
15. Du, Y.Y., Wang, P.C., Chen, J. Song, C.P. (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J. Integr. Plant Biol. 50, 1318 1326.
16. Foyer, C.H. Noctor, G. (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant. 119, 355 364.
17. Foyer, C.H., Noctor, G., Buchanan, B., Dietz, K.J. Pfannschmidt, T. (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861 905.
18. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S. Mullineaux, P.M. (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819 832.
19. Huang, A.H.C., Trelease, R.N. Moore, T.S. (1983) Plant Peroxisomes.
20. Jimenez, A., Hernandez, J.A., Pastori, G., del Rio, L.A. Sevilla, F. (1998a) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol. 118, 1327 1335.
21. Jiménez, A., Hernández, J.A., Ros Barceló, A., Sandalio, L.M., del Río, L.A. Sevilla, F. (1998b) Mitochondrial and peroxisomal ascorbate peroxidase of pea leaves. Physiol. Plant. 104, 687 692.
22. Lasorsa, F.M., Pinton, P., Palmieri, L., Scarcia, P., Rottensteiner, H., Rizzuto, R. Palmieri, F. (2008) Peroxisomes as novel players in cell calcium homeostasis. J. Biol. Chem. 283, 15300 15308.
23. Locato, V., de Pinto, M.C. De Gara, L. (2009) Different involvement of the mitochondrial, plastidial and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Physiol Plant. 135, 296 306.
24. McClung, C.R. (1997) Regulation of catalases in Arabidopsis. Free Radic. Biol. Med. 23, 489 496.
25. Mittler, R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405 410.
26. Murashige, T. Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473 497.
27. 2+. Proc. Natl Acad. Sci. USA, 98, 3197 3202.
28. Narendra, S., Venkataramani, S., Shen, G., Wang, J., Pasapula, V., Lin, Y., Kornyeyev, D., Holaday, A.S. Zhang, H. (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J. Exp. Bot. 57, 3033 3042.
29. Noh, Y.S. Amasino, R.M. (1999) Identification of a promoter region responsible for the senescence specific expression of SAG12. Plant Mol. Biol. 41, 181 194.
30. Nyathi, Y. Baker, A. (2006) Plant peroxisomes as a source of signalling molecules. Biochim. Biophys. Acta, 1763, 1478 1495.
31. Orendi, G., Zimmermann, P., Baar, C. Zentgraf, U. (2001) Loss of stress-induced expression of catalase3 during leaf senescence in Arabidopsis thaliana is restricted to oxidative stress. Plant Sci. 161, 301 314.
32. Palma, J.M., Corpas, F.J. Del Río, L.A. (2009) Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics, 9, 2301 2312.
33. 2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem. Biol. 13, 521 530.
34. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G.J., Grill, E. Schroeder, J.I. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406, 731 734.
35. Queval, G., Issakidis-Bourguet, E., Hoeberichts, F.A., Vandorpe, M., Gakière, B., Vanacker, H., Miginiac-Maslow, M., Van Breusegem, F. Noctor, G. (2007) Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J. 52, 640 657.
36. Reumann, S., Ma, C., Lemke, S. Babujee, L. (2004) AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol. 136, 2587 2608.
37. del Río, L.A., Pastori, G.M., Palma, J.M., Sandalio, L.M., Sevilla, F., Corpas, F.J., Jiménez, A., López-Huertas, E. Hernández, J.A. (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol. 116, 1195 1200.
38. del Río, L.A., Corpas, F.J., Sandalio, L.M., Palma, J.M., Gómez, M. Barroso, J.B. (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J. Exp. Bot. 53, 1255 1272.
39. del Río, L.A., Sandalio, L.M., Corpas, F.J., Palma, J.M. Barroso, J.B. (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol. 141, 330 335.
40. Rudolf, R., Mongillo, M., Rizzuto, R. Pozzan, T. (2003) Looking forward to seeing calcium. Nat. Rev. Mol. Cell Biol. 4, 579 586.
41. Schulte, A., Lorenzen, I., Böttcher, M. Plieth, C. (2006) A novel fluorescent pH probe for expression in plants. Plant Methods, 6, 2 7.
42. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y. Yoshimura, K. (2002) Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53, 1305 1319.
43. Wadsworth, G.J. Scandalios, J.G. (1989) Differential expression of the maize catalase genes during kernel development: the role of steady-state mRNA levels. Dev. Genet. 10, 304 310.
44. 2 and is indispensable for stress defence in C3 plants. EMBO J. 15, 4806 4816.
45. Yang, T. Poovaiah, B.W. (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc. Natl Acad. Sci. USA, 99, 4097 4102.
46. Yang, Y., Costa, A., Leonhardt, N., Siegel, R.S. Schroeder, J.I. (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods, 19, 4 6.
47. 2 insensitivity of the gca2 mutant. Proc. Natl Acad. Sci. USA, 103, 7506 7511.
48. Zentgraf, U. (2007) Oxidative stress and leaf senescence. In Senescence Processes in Plants Annual Plant Reviews.
49. Zimmermann, P., Heinlein, C., Orendi, G. Zentgraf, U. (2006) Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ. 29, 1049 1060.
50. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D., Boller, T. Felix, G. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell, 125, 749 760.